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FOLIA POMERANAE UNIVERSITATIS TECHNOLOGIAE STETINENSIS

Folia Pomer. Univ. Technol. Stetin., Agric., Aliment., Pisc., Zootech. 2014, 309 (29), 25–40

Lidia FELSKA-BŁASZCZYK, Piotr BARANOWSKI, Katarzyna PĘZIŃSKA-KIJAK,

Piotr NOWAK, Olga STELTER

1

THE ASYMMETRY OF SELECTED SKELETON ELEMENTS IN RED FOX

(VULPES VULPES) AND RACCOON DOG (NYCTEREUTES PROCYONOIDES),

BOTH WILD AND FARMED

ASYMETRIA WYBRANYCH ELEMENTÓW SZKIELETU LISA POSPOLITEGO

(VULPES VULPES) I JENOTA (NYCTEREUTES PROCYONOIDES) DZIKIEGO

I HODOWLANEGO

Laboratory of Animal Anatomy, Faculty of Biotechnology and Animal Science, West Pomeranian University of Technology, Szczecin, Poland

Streszczenie. Celem badań było określenie wpływu pochodzenia i płci zwierząt na występowanie symetrii lub asymetrii wybranych elementów szkieletu kończyny piersiowej lisa pospolitego dzikiego i hodowlanego oraz jenota dzikiego i hodowlanego. Badania przeprowadzono na 20 osobnikach lisa pospolitego hodowlanego (10 samców i 10 samic) i 24 osobnikach lisa dzikiego (15 samców i 9 samic) oraz na 20 osobnikach jenota hodowlanego (10 samic i 10 samców) i 12 osobnikach jenota dzikiego (6 samic i 6 samców). Od wszystkich osobników wypreparowano elementy prawej i lewej kończyny obręczy piersiowej (cingulum membri thoracici) – łopatkę (scapula) oraz kościec części wolnej kończyny piersiowej reprezentowany przez kość ramienną (humerus), kość promieniową (radius) i kość łokciową (ulna). Kości zostały zmierzone za pomocą suwmiarki elektronicznej. W wyniku przeprowadzonych badań stwierdzono, że asymetria kości kończyny przedniej występuje sporadycznie i zasadniczo u zwierząt hodowlanych. Na wszystkie analizowane cechy metryczne wybranych kości miały wpływ badane źródła zmienności (pochodzenie zwierząt oraz płeć). W kości ramiennej lisów pospolitych stwierdzono asymetrię lewostronną, która występowała również w pozostałych elementach szkieletu. Przeprowadzone badania skłaniają do stwierdzenia, że utrzymanie zwierząt w warunkach hodowli stabulacyjnej może mieć wpływ na pojawianie się zjawiska asymetrii szkieletu w obręczy piersiowej.

Key words: domestication, fluctuating asymmetry, humerus, radius, relative asymmetry, scapula, ulna.

Słowa kluczowe: asymetria fluktuacyjna, asymetria względna, domestykacja, humerus, radius, scapula, ulna.

INTRODUCTION

The red fox is one of the world's most common carnivore (Vos 1995; Cavallini 1996;

Cavallini and Santini 1996; Gortázar et al. 2003; Aubry et al. 2009). The first farm of red

foxes were started in the nineteenth century, so the history of red fox breeding is more than

Corresponding autor – Adres do korespondencji: PhD Lidia Felska-Błaszczyk, Laboratory of Animal Anatomy, Faculty of Biotechnology and Animal Science, West Pomeranian University of Technology, Szczecin, Doktora Judyma 14, 71-466 Szczecin, Poland, e-mail: lidia.felska-blaszczyk@zut.edu.pl

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26 L. Felska-Błaszczyk et al.

120 years old. Raccoon dog breeding, on the other hand, does not have such a long

tradition, and in Poland it has been carried out for about 50 years. The first attempts to farm

this species took place in Russia (Gugołek 2013). Raccoon dog was brought to Europe

between the years 1927–1957, and some animals were released into the wild for hunting

purposes, and some allocated to farming farmed game (Kowalczyk et al. 2009; Święcicka

et al. 2011; Mohammad Nafi Solaiman Al-Sabi et al 2013; Gugołek 2013). Currently, the

raccoon dog occurs is a part of the ecosystem across the entire Northern and Central Europe.

Farming has induced a number of changes in the morphology and etiology of the red fox

and, as a result, many differences exist between red foxes from the wild population and

those bred on farms. For example, farmed foxes are characterized by a heavier body weight

and shorter length compared to the wild-living red foxes (Felska-Błaszczyk et al. 2013).

Forelimbs are significantly longer in farmed foxes. Wild foxes also show a considerable

obliteration of sexual dimorphism within some skeletal characters (Felska-Błaszczyk et al. 2013).

Besides morphology, farmed foxes differ in terms behavior from their wild kins. As a result of

farming, the foxes have gradually lost the ability hunting, movement and orientation in the

wild (O’Regan and Kitchener 2005). Wild foxes are also characterized by a stronger

environmental and genetic variability (Cavallini 1997; Nowicki 2005).

Farmed animals are managed under relatively constant conditions, under the stability that

is unknown in nature. Food availability, cage sizes, and selection are the factors that alter not

only body size, but also may impose asymmetry in various morphological characters.

Fluctuating asymmetry, which reflects the effects of environmental conditions on the bilateral

traits f the skeleton (Siegel et al. 1977), can represent a measure of environmental impact in

terms of the body symmetry (Hallgrimsson 1993; Graham et al. 1994; Tomkins and Kotiaho 2001).

A certain degree of asymmetry in the body can be a result of various environmental factors

that shape the final phenotypic image of the individual. It can be used for evaluating the

adaptation and effects of living conditions on the organism. The degree of asymmetry can be

used in studies on genotype-environment interactions and demonstrates whether the

environment of the animals – natural or on-farm – is of an effect in terms of bilateral differences

in morphology. Relative body asymmetry is another measure showing differences between

the left and the right side of the body (Henneberg 1974; Baranowski and Wojtas 2011).

The aim of the study was to determine the effect of origin on the presence of asymmetry

in selected bones of the forelimb of the red fox and raccoon dog living in different

environments: natural and farm.

MATERIAL AND METHODS

The study involved 20 farmed red foxes (10 males and 10 females), 24 wild foxes (15 males

and 9 females), 20 farmed raccoon dogs (10 males and 10 females), and 12 wild raccoon

dogs (6 males and 6 females). The animals were collected in southern Poland; the wild foxes

and raccoon dogs were captured in restraining traps, and the farmed animals were obtained

from a fur farm. The following right- and left-side skeletal parts were dissected from all

individuals: the shoulder blade (scapula) of the pectoral girdle (cingulum membri thoracici)

and the thoracic limb bones, the humerus, the radius, and the ulna. Each bone underwent

bilateral measurements using the methodology drawn from studies by Alpak et al. (2004) and

Monchot and Gendron (2010).

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The asymmetry of selected$ 27

The humerus was measured for the following morphometric characters: greatest length

(GL), greatest length of the lateral part (GLI, from the cranial part of the lateral tuberosity to

the most distal point of the lateral border of the trochlea), greatest length from caput (GLC),

greatest breadth of the proximal end (BP), greatest breadth of the distal end (BD), greatest

breadth of the trochlea (BT) smallest breadth of diaphysis (SD). The radius was measured

for: greatest length (GL), greatest breadth of the proximal end (BP), greatest breadth of the

distal end (BD), smallest breadth of diaphysis (SD). The ulna: greatest length (GL), smallest

depth of the olecranon (SDO), depth across the anconeal process (DPA). The scapula:

greatest dorsal length (LD), height along the spine (HS, external length of the scapula),

diagonal height (DHA), smallest length of the collum scapulae (SCL), greatest length of the

glenoid process (GLP).

The resulting data were processed statistically using Statistica v.10.0 PL package.

Arithmetic mean, standard deviation (SD), and the coefficient of variability (V%) were

calculated. To determine the effect of origin and sex between the averages in each

measurement, nonparametric Mann-Whitney U-test was used. The effects of origin, sex, and

the body was calculated using an F test of asymmetry relative values (AW) and fluctuating

asymmetry (FA) was estimated by the following equations (Henneberg 1974), whose

formulas are shown below:

(

)

l

l

r

=

RA

×

100

Where:

RA – relative asymmetry,

r

– right-side mean,

l

– left-sie mean.

varl

varr

l

varr

=

FA

×

Where:

FA – fluctuating asymmetry,

r – right-side,

l – left-side.

Positive values of both relative and fluctuating asymmetry denote right-side asymmetry,

while negative – left-side asymmetry. To determine the effect of differences between the

characters depending on which side of the body they are located, we used the sign test and

Wilcoxon matched pairs test.

RESULTS AND DISCUSSION

Table 1 presents the effect of selected sources of variability on some characters of

pectoral girdle bones in the red fox. We found a significant effect of origin (wild vs. farmed

foxes) on three characters in the scapula, four in the humerus and radius, and one in the

ulna. Sex of the foxes was a significant source od variability in the case of all the traits in the

studied bones. We did not, on the other hand, find a statistically significant effect of the side

of the body on the studied traits. Interactions estimated for origin and sex of the studied

bones were significant (P ≤ 0.05 and P ≤ 0.01) for 12 out of 19 studied characters of the

bones of the pectoral girdle.

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28 L. Felska-Błaszczyk et al.

Table 1. Sources of variability included in the linear model and estimation of their effect on the paramters of pectoral girdle and forelimb bones in the red fox

Tabela 1. Efekty uwzględnione w modelu liniowym i ocena ich wpływu na parametry kości obręczy przedniej lisa pospolitego

Trait – Cecha Wpływ pochodzenia Effect of origin Effect of sex Wpływ płci Effect of the body side Wpływ strony ciała Interactions Interakcje SCAPULA – ŁOPATKA LD 095.27** 060.66** 0.16 11.13** † HS 008.85** 104.27** 0.18 0.02-0.60 DHA 003.45** 113.31** 0.13 0.00–0.32 SCL 005.93** 036.80** 0.00 4.93* † GLP 000.56** 100.47** 3.39 7.58** †

HUMERUS – KOŚĆ RAMIENNA

GL 042.45** 142.31** 0.10 3.38* † GLI 046.38** 131.24** 0.12 5.13* † GLC 039.88** 120.31** 0.06 4.30* † BP 001.07** 052.37** 3.85 8.11** † BD 001.00** 057.81** 0.00 0.16–0.35 BT 000.49** 015.36** 0.24 0.01–0.76 SD 013.24** 027.84** 0.28 17.29** †

RADIUS – KOŚĆ PROMIENIOWA

GL 028.57** 137.21** 0.04 7.75** †

BP 005.62** 055.84** 0.37 0.11–3.54

BD 007.98** 057.82** 0.04 8.55** †

SD 136.73** 006.49*0 0.03 21.45** †

ULNA – KOŚĆ ŁOKCIOWA

GL 026.02** 103.61** 0.43 8.19** †

SDO 003.29** 043.74** 0.04 0.03–2.75 DPA 000.08** 036.82** 1.19 0.00–0.90 Explanations: column “Interactions” contain interaction value or its range;

† – interaction: origin × sex,

** – statistical significance at P ≤ 0.01, * – statistical significance P ≤ 0.05.

Objaśnienia: w kolumnie „Interakcje” wpisano wartości interakcji lub zakres wartości interakcji; † – interakcja: pochodzenie × płeć,

** – wpływ statystyczny czynnika na poziomie P ≤ 0,01, * – wpływ statystyczny czynnika na poziomie P ≤ 0,05.

Tables 2–5 present the statistical characterization of the traits of the scapula, humerus,

radius, and the ulna of females and males of the red fox. We found significant (P ≤ 0.05 and

P ≤ 0.01) bilateral differences, confirmed by a significant (P ≤ 0.05) value of the sign test, for

such traits as:

the height along the spine (HS) of the scapulae in farmed fox females,

the greatest breadth of the trochlea (BT) of wild fox females,

the greatest breadth of the proximal end (BP) of the radius in farmed fox females, and

the greatest breadth of the distal end (BD).

None of the three studied morphometric characters of the ulna, either in males or females

of the red fox, showed a significant bilateral difference.

The skeletal elements of the pectoral girdle in raccoon dogs showed a significant effect of

origin on most of the characters included in the analysis (Table 6). No statistically significant

effect of origin (natural or farm conditions) was found in relation to the smallest length of the

collum scapulae (SCL), greatest breadth of the proximal end (BP) or the smallest breadth of

diaphysis (SD).

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Table 2. Statistical characteristics of the scapula morphometrics in the red fox Tabela 2. Charakterystyka statystyczna wymiarów łopatki lisa pospolitego

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ LD Farmed fox Lis hodowlany F L 50.75 2.32 4.58 0.00 0.102 0.721 0.752 R 50.75 2.44 4.82 M L 52.82 1.73 3.26 0.57 0.247 0.445 0.752 R 53.12 1.96 3.69 Wild fox Lis dziki F L 43.88 1.10 2.52 1.62 0.601 0.500 1.000 R 44.59 1.48 3.33 M L 49.87 2.16 4.34 –0.41 0.109 0.551 0.423 R 49.67 2.29 4.60 HS Farmed fox Lis hodowlany F L 82.59 1.35 1.63 1.09 0.544 0.005** 0.004** R 83.49 1.76 2.11 M L 88.17 1.16 1.31 0.46 0.221 0.047* 0.114 R 88.57 1.29 1.46 Wild fox Lis dziki F L 81.31 2.14 2.63 –0.37 0.273 0.249 0.683 R 81.01 2.39 2.95 M L 87.04 3.38 3.89 –0.09 –0.118 0.754 0.789 R 86.95 3.19 3.67 DHA Farmed fox Lis hodowlany F L 82.00 1.78 2.17 0.18 0.125 0.476 0.752 R 82.15 1.89 2.30 M L 87.32 1.77 2.03 0.68 –0.646 0.114 0.343 R 87.91 1.29 1.47 Wild fox Lis dziki F L 80.80 1.61 1.99 –0.16 0.883 0.046* 0.221 R 80.67 2.46 3.05 M L 86.81 3.10 3.57 0.23 0.087 0.311 1.000 R 87.01 3.24 3.72 SCL Farmed fox Lis hodowlany F L 15.27 0.42 2.76 0.58 –0.118 0.386 0.752 R 15.36 0.39 2.57 M L 16.11 0.67 4.15 1.47 –0.315 0.074 0.114 R 13.35 0.57 3.51 Wild fox Lis dziki F L 15.40 0.98 6.35 –0.52 –0.147 0.600 0.683 R 15.32 0.91 5.92 M L 17.43 1.39 7.97 –1.06 3.000 0.132 0.181 R 17.24 1.59 9.22 GLP Farmed fox Lis hodowlany F L 17.63 0.38 2.16 –1.24 0.660 0.169 0.343 R 17.41 0.39 2.25 M L 18.61 0.41 2.20 –0.44 –0.357 0.508 0.752 R 18.53 0.34 1.87 Wild fox Lis dziki F L 17.46 0.72 4.16 –2.62 0.074 0.249 0.683 R 17.00 0.75 4.42 M L 19.24 0.85 4.41 –1.62 –0.134 0.026* 0.061 R 18.93 0.79 4.20 Explanations: – Objaśnienia:

F – female – samica; M – male – samiec; L – left body side – L strona ciała; R – right body side – prawa strona ciała; RA – Relative asymmetry value – wartości wskaźnika asymetrii względnej; FA – fluctuating asymmetry value – wartości wskaźnika asymetrii fluktuacyjnej; TpW – Wilcoxon test value – wartość testu Wilcoxona; TZ – sign test value – wartość testu znaków;

** Wilcoxon test or sign test value significant at P ≤ 0.01 – wartość testu Wilcoxona lub testu znaków istotna przy P ≤ 0,01;

* Wilcoxon test or sign test value significant at P ≤ 0.05 – wartość testu Wilcoxona lub testu znaków istotna przy P ≤ 0,05.

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Table 3. Statistical characteristics of the humerus morphometrics in the red fox Tabela 3. Charakterystyka statystyczna wymiarów kości ramiennej lisa pospolitego

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed fox Lis hodowlany F L 126.79 5.71 4.50 1.26 –1.416 0.285 0.752 R 128.39 2.95 2.30 M L 136.88 3.99 2.91 –0.25 –0.278 0.139 0.343 R 136.54 3.47 2.54 Wild fox Lis dziki F L 119.72 3.97 3.32 –1.49 –0.265 0.686 1.000 R 117.93 3.48 2.95 M L 133.18 4.29 3.22 –0.51 –0.087 0.937 0.386 R 132.50 4.11 3.10 GLI Farmed fox Lis hodowlany F L 125.52 5.65 4.50 1.04 –1.302 0.799 0.752 R 126.83 3.06 2.42 M L 135.16 3.77 2.79 –0.03 0.013 0.721 0.752 R 135.11 3.80 2.81 Wild fox Lis dziki F L 118.27 4.26 3.60 –1.58 –0.437 0.500 0.371 R 116.40 3.43 2.94 M L 131.07 4.30 3.28 –0.55 –0.124 0.814 0.773 R 130.34 4.04 3.10 GLC Farmed fox Lis hodowlany F L 123.83 6.98 5.63 1.60 –1.822 0.285 0.752 R 125.80 3.08 2.45 M L 134.08 4.28 3.20 –0.09 –0.255 0.799 0.752 R 133.96 3.77 2.82 Wild fox Lis dziki F L 117.20 4.15 3.54 –1.82 –0.337 0.584 0.617 R 115.06 3.51 3.05 M L 129.98 4.16 3.20 –0.54 –0.141 0.790 1.000 R 129.28 3.87 3.00 BP Farmed fox Lis hodowlany F L 18.11 a 1.18 6.51 –4.04 –2.420 0.047* 0.114 R 17.38a 0.42 2.43 M L 18.70 0.49 2.63 –2.25 –0.181 0.037* 0.114 R 18.28 0.45 2.49 Wild fox Lis dziki F L 17.46 0.79 4.56 –0.27 0.090 0.249 0.221 R 17.42 0.83 4.79 M L 19.22 0.73 3.79 –0.69 0.018 0.177 0.423 R 19.08 0.73 3.84 BD Farmed fox Lis hodowlany F L 20.33 0.54 2.64 1.36 0.000 0.169 0.114 R 20.61 0.53 2.59 M L 21.77 0.41 1.87 –0.30 0.523 0.721 0.752 R 21.70 0.53 2.43 Wild fox Lis dziki F L 20.24 0.77 3.82 –0.60 –0.052 0.917 0.683 R 20.12 0.75 3.73 M L 21.70 1.05 4.82 –0.34 0.053 0.507 1.000 R 21.63 1.07 4.97 BT Farmed fox Lis hodowlany F L 12.69 0.43 3.43 3.12 –0.285 0.022* 0.114 R 13.09 0.50 3.79 M L 13.71 0.31 2.24 –0.08 0.500 0.959 0.752 R 13.70 0.39 2.89 Wild fox Lis dziki F L 12.92 0.63 4.86 1.46 –0.054 0.028* 0.041* R 13.11 0.61 4.67 M L 13.96 0.64 4.61 –1.12 2.655 0.397 0.789 R 13.80 1.91 13.85 SD Farmed fox Lis hodowlany F L 7.70 0.47 6.06 –0.94 0.130 0.214 0.505 R 7.63 0.50 6.52 M L 7.80 0.36 4.63 –0.91 –0.400 0.093 0.114 R 7.73 0.31 3.98 Wild fox Lis dziki F L 7.62 0.52 6.81 –0.09 –2.000 0.345 0.221 R 7.61 0.22 2.96 M L 8.53 0.42 4.93 –0.57 –0.125 0.363 0.423 R 8.48 0.40 4.69

Explanations: mean marked with lower-case letters differ in cilumns significantly at P ≤ 0.05; * – Wilcoxon test and sign test value significant at P ≤ 0.05.

Objaśnienia: średnie oznaczone w kolumnach małymi literami różnią się istotnie P ≤ 0,05; *– wartość testu par Wilcoxona i testu znaków istotna na poziomie P ≤ 0,05.

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Table 4. Statistical characteristics of the radius morphometrics in the red fox

Tabela 4. Charakterystyka statystyczna wymiarów kości promieniowej lisa pospolitego

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed fox Lis hodowlany F L 120.14 2.22 1.85 0.22 –0.085 0.126 0.114 R 120.41 2.13 1.77 M L 127.97 3.30 2.58 –0.10 –0.049 0.878 0.752 R 127.84 3.22 2.52 Wild fox Lis dziki F L 113.50 2.25 1.98 –0.29 1.298 0.068 0.134 R 113.15 4.13 3.65 M L 125.27 4.22 3.37 –0.70 10.73 0.638 0.773 R 126.16 4.51 3.57 BP Farmed fox Lis hodowlany F L 11.05 0.37 3.39 2.89 –0.888 0.009** 0.027* R 11.37 0.25 2.22 M L 11.74 0.24 2.09 0.42 0.333 0.541 0.752 R 11.79 0.29 2.47 Wild fox Lis dziki F L 11.33 0.48 4.28 –1.23 -– 1.214 0.753 0.683 R 11.19 0.59 5.30 M L 12.18 0.47 3.84 5.00 0.346 0.917 1.000 R 12.18 0.56 4.60 BD Farmed fox Lis hodowlany F L 14.64 0.43 2.93 1.09 0.333 0.059 0.114 R 14.81 0.50 3.41 M L 15.27 0.49 3.18 1.50 –0.238 0.051 0.182 R 15.50 0.43 2.80 Wild fox Lis dziki F L 14.70 0.83 5.63 20.47 –0.193 0.043* 0.074 R 14.71 0.75 5.13 M L 16.34 0.77 4.69 –0.37 –0.590 0.006** 0.016* R 16.04 0.57 3.58 SD Farmed fox Lis hodowlany F L 7.12 0.57 8.07 –1.12 0.194 0.594 1.000 R 7.04 0.63 9.01 M L 6.86 0.50 7.26 –1.45 0.000 0.333 0.752 R 6.76 0.50 7.45 Wild fox Lis dziki F L 7.91 0.76 9.57 –9.73 –1.058 0.116 0.683 R 8.05 0.46 5.68 M L 8.93 0.48 5.38 0.56 0.370 0.490 0.789 R 8.88 0.57 6.47

For explanations see Table 2. Objaśnienia jak w tabeli 2.

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Table 5. Statistical characteristics of the ulna morphometrics in the red fox Tabela 5. Charakterystyka statystyczna wymiarów kości łokciowej lisa pospolitego

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed fox Lis hodowlany F L 140.35 2.53 1.80 0.33 0.057 0.047* 0.114 R 140.82 2.60 1.85 M L 148.82 3.80 2.55 –0.12 0.013 0.508 0.343 R 148.64 3.82 2.57 Wild fox Lis dziki F L 132.74a 2.93 2.21 –1.53 9.965 0.068 0.134 R 130.71a 7.99 6.11 M L 146.83b 5.52 3.76 0.12 –0.232 0.552 1.000 R 145.65b 4.91 3.37 SDO Farmed fox Lis hodowlany F L 12.44 0.53 4.25 0.64 0.000 0.203 0.114 R 12.52 0.53 4.26 M L 13.36 0.72 5.39 –1.42 –0.524 0.037* 0.343 R 13.18 0.73 5.51 Wild fox Lis dziki F L 12.48 0.83 6.66 0.48 0.338 0.345 0.683 R 12.53 0.88 7.01 M L 13.86 0.69 4.99 0.50 0.364 0.315 0.789 R 13.79 0.67 4.86 DPA Farmed fox Lis hodowlany F L 14.90 0.58 3.87 2.21 –0.56 0.032* 0.114 R 15.23 0.44 2.86 M L 15.74 0.43 2.71 1.33 3.052 0.203 0.752 R 15.95 0.47 2.93 Wild fox Lis dziki F L 14.97 0.74 4.93 –0.06 –3.960 0.345 0.221 R 14.96 0.70 4.67 M L 15.96 0.80 4.99 0.87 0.200 0.029* 0.096 R 16.10 0.85 5.27

Explanations: mean marked with same upper-case letters differ in columns significantly at P ≤ 0.01; lower-case letters: at P ≤ 0.05; ** – Wilcoxon test and sign test value significant at P ≤ 0.01; * – Wilcoxon test and sign test value significant at P ≤ 0.05.

Objaśnienia: średnie oznaczone w kolumnach: tymi samymi wielkimi literami różnią się istotnie P ≤ 0,01; małymi literami – P ≤ 0,05; ** – wartość testu Wilcoxona lub testu znaków istotna przy P ≤ 0,01; * – wartość testu Wilcoxona lub testu znaków istotna przy P ≤ 0,05.

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The asymmetry of selected$ 33 Table 6. Sources of variability included in the linear model and estimation of their effect significance

on the parameters of pectoral girdle and forelimb bones in the raccoon dog

Tabela 6. Efekty uwzględnione w modelu liniowym i ocena ich istotności wpływu na parametry kości obręczy przedniej jenota

Trait Cecha Effect of origin Wpływ pochodzenia Effect of sex Wpływ płci

Effect of body side Wpływ strony ciała

Interactions Interakcje SCAPULA – ŁOPATKA LD 005.82* 0.36 0.04 7.49** † HS 019.22** 1.26 0.00 0.04-0.86 DHA 016.07** 0.65 0.16 7.00* † SCL 002.01 0.07 0.31 7.20** † GLP 014.57** 4.10* 1.83 0.38–1.83

HUMERUS – KOŚĆ RAMIENNA

GL 013.35** 1.01 0.05 0.22–2.91 GLI 014.70** 1.52 0.02 0.22–2.92 GLC 009.38** 3.97 0.27 0.06–3.76 BP 000.36 0.06 0.72 0.73–2.01 BD 043.67** 1.51 0.00 0.00–0.93 BT 067.44** 0.33 0.08 0.00–0.41 SD 002.40 2.24 0.01 0.02–3.82

RADIUS – KOŚĆ PROMIENIOWA

GL 037.92** 1.09 0.78 0.26–2.85

BP 074.40** 2.68 0.04 0.03–1.02

BD 0 5.87* 9.34** 0.68 0.00–0.02

SD 037.36** 2.89 0.23 0.09–0.74

ULNA – KOŚĆ ŁOKCIOWA

GL 037.75** 9.54** 0.04 0.00–0.07

SDO 065.78** 1.86 3.55 0.02–1.07

DPA 276.59** 0.88 0.04 0.02–1.31

For explanations see Table 1. Objaśnienia jak w tabeli 1.

The effect of sex was significant (P ≤ 0.05) only in relation to the greatest length of the

glenoid process (GLP) in the scapula, the greatest breadth of the distal end (BD) of the

radius (P ≤ 0.01), and the greatest length of the ulna (GL). If we look into the bilateral

characters of the skeletal elements of the pectoral girdle in raccoon dogs, no statistically

significant effect of the side of the body can be found. The estimated values of origin × sex

interactions included in the statistical analysis were significant (P ≤ 0.05 and P ≤ 0.01) only

for three scapular characters: the greatest dorsal length (LD), diagonal height (DHA), and the

smallest length of the collum scapulae (SCL).

Statistical characterization of scapulae measurements in farmed raccoon dogs

demonstrates its bilateral relationship for the greatest length of the glenoid process (GLP).

The matched pairs values estimated using the Wilcoxon test reveal a significant (P ≤ 0.01)

left-sided asymmetry, which was confirmed by the sign test. Also in the females of farmed

raccoon dogs, the estimated right-sided asymmetry in the smallest depth of the olecranon

(SDO) was significant (P ≤ 0.01) and confirmed by the sign test (P ≤ 0.05). The remaining

characters of the skeleton of the pectoral girdle in both farmed and wild raccoon dogs did not

show any differences in the morphometric values which could have been confirmed by the

applied tests.

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Table 7. Statistical characteristics of the scapula morphometrics in the raccoon dog Tabela 7. Charakterystyka statystyczna wymiarów łopatki jenota

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ LD Farmed raccoon dog Jenot hodowlany F L 42.59 1.94 4.54 0.68 –0.279 0.575 0.752 R 42.88 1.69 3.93 M L 44.00 1.82 4.14 0.43 –0.369 0.386 0.752 R 44.19 1.52 3.44 Wild raccoon dog Jenot dziki F L 46.14 3.57 7.75 –0.57 –0.174 0.593 1.000 R 45.87 3.21 6.99 M L 43.74 2.61 5.96 0.65 0.095 0.361 0.617 R 44.03 2.73 6.21 HS Farmed raccoon dog Jenot hodowlany F L 83.96 2.06 2.45 0.07 0.126 0.799 0.752 R 84.01 2.19 2.61 M L 86.07 7.11 8.26 0.79 –3.770 0.919 0.752 R 86.75 1.77 2.04 Wild raccoon dog Jenot dziki F L 80.48 5.92 7.36 –1.44 –0.978 0.593 1.000 R 79.32 3.70 4.66 M L 79.93 3.27 4.09 0.49 –0.006 0.068 0.134 R 80.32 3.26 4.06 DHA Farmed raccoon dog Jenot hodowlany F L 81.71 2.46 3.01 0.64 0.292 0.074 0.114 R 82.23 2.13 2.59 M L 84.58 1.57 1.86 –0.08 0.073 0.919 0.752 R 84.51 1.63 1.93 Wild raccoon dog Jenot dziki F L 81.39 2.86 3.51 –1.07 0.334 0.593 1.000 R 80.52 3.38 4.20 M L 79.98 3.49 4.36 –0.97 0.445 0.465 0.617 R 79.20 4.35 5.49 SCL Farmed raccoon dog Jenot hodowlany F L 16.15 0.63 3.90 0.34 –0.052 0.838 0.752 R 16.21 0.62 3.82 M L 16.60 0.51 3.08 –0.02 0.000 0959 0.752 R 16.60 0.51 3.08 Wild raccoon dog Jenot dziki F L 16.33 0.48 2.92 0.89 –0.687 1.000 1.000 R 16.47 0.34 2.09 M L 15.79 0.65 4.12 1.23 0.537 0.715 0.617 R 15.98 0.85 5.30 GLP Farmed raccoon dog Jenot hodowlany F L 18.51 0.57 3.08 –2.40 0.333 0.005** 0.004** R 18.07 0.65 3.60 M L 18.68 0.43 2.32 –1.73 –0.400 0.047* 0.114 R 18.35 0.35 1.93 Wild raccoon dog Jenot dziki F L 17.47 0.76 4.35 1.35 –8.142 0.593 1.000 R 17.70 0.09 0.54 M L 18.17 0.60 3.30 –1.81 0.250 0.068 0.134 R 17.84 0.68 3.79

Explanations: ** – Wilcoxon test or sign test value significant at P ≤ 0.01; * – Wilcoxon test or sign test value significant at P ≤ 0.05.

Objaśnienia: ** – wartość testu par Wilcoxona lub testu znaków istotna przy P ≤ 0,01; * – wartość testu par Wilcoxona lub testu znaków istotna przy P ≤ 0,05.

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Table 8. Statistical characteristics of the humerus morphometrics in the raccoon dog Tabela 8. Charakterystyka statystyczna wymiarów kości ramiennej jenota

Trait Cecha

Origin

Pochodzenie Płeć Sex

Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed raccoon dog Jenot hodowlany F L 99.49 1.72 1.73 –0.48 0.389 0.114 0.752 R 99.01 2.09 2.11 M L 100.91 2.66 2.64 0.29 –0.035 0.139 0.114 R 101.21 2.62 2.59 Wild raccoon dog Jenot dziki F L 97.42 3.58 3.67 –0.23 –0.179 0.465 0.617 R 97.18 3.28 3.37 M L 97.26 3.84 3.95 1.07 0.308 0.500 1.000 R 96.96 4.48 4.62 GLI Farmed raccoon dog Jenot hodowlany F L 97.91 1.56 1.59 –0.33 –0.504 0.093 0.343 R 97.58 2.00 2.05 M L 99.35 2.73 2.75 0.28 –0.025 0.445 0.752 R 99.63 2.70 2.71 Wild raccoon dog Jenot dziki F L 95.54 3.71 3.88 0.01 –0.200 0.715 0.617 R 95.56 3.34 3.50 M L 95.91 3.73 3.89 –0.38 –0.119 0.080 0.371 R 95.54 3.51 3.67 GLC Farmed raccoon dog Jenot hodowlany F L 97.53 1.81 1.86 –0.22 0.607 0.683 0.752 R 97.30 2.45 2.51 M L 99.08 2.88 2.90 0.47 0.184 0.241 0.752 R 99.55 3.15 3.17 Wild raccoon dog Jenot dziki F L 95.15 3.59 3.78 –0.05 –0.166 0.715 0.617 R 95.10 3.31 3.48 M L 97.49 2.43 2.49 –1.96 1.308 0.686 1.000 R 95.57 4.49 4.70 BP Farmed raccoon dog Jenot hodowlany F L 17.94 0.79 4.40 –1.50 –0.387 0.139 0.343 R 17.67 0.65 3.69 M L 18.30 0.48 2.61 –2.51 0.428 0.037* 0.343 R 17.84 0.59 3.30 Wild raccoon dog Jenot dziki F L 17.70 0.36 2.03 2.59 0.153 0.068 0.134 R 18.16 0.39 2.13 M L 17.89 0.54 3.03 –1.67 –0.500 0.345 0.074 R 17.59 0.42 2.38 BD Farmed raccoon dog Jenot hodowlany F L 22.45 0.90 4.01 –0.35 –0.373 0.610 0.343 R 22.36 0.74 3.33 M L 22.80 0.24 1.05 0.35 1.846 0.953 1.000 R 22.88 0.55 2.41 Wild raccoon dog Jenot dziki F L 21.30 0.55 2.58 0.04 –0.107 0.715 0.617 R 21.31 0.52 2.44 M L 21.34 0.86 4.05 0.14 0.113 0.686 1.000 R 21.37 0.92 4.30 BT Farmed raccoon dog Jenot hodowlany F L 15.16 0.90 5.96 –0.19 –0.461 0.878 0.752 R 15.13 0.72 4.75 M L 14.77 1.00 6.81 3.11 –0.742 0.028* 0.114 R 15.23 0.70 4.59 Wild raccoon dog Jenot dziki F L 13.27 0.73 5.51 –0.37 0.135 0.465 0.617 R 13.22 0.79 5.95 M L 13.18 0.61 4.61 –0.83 0.325 0.893 1.000 R 13.07 0.72 5.49 SD Farmed raccoon dog Jenot hodowlany F L 7.89 0.43 5.54 0.38 –0.250 0.799 0.752 R 7.81 0.38 4.89 M L 8.22 0.37 4.47 –0.65 –0.076 0.139 0.343 R 8.14 0.37 4.50 Wild raccoon dog Jenot dziki F L 8.18 0.17 2.10 0.24 2.375 1.000 0.617 R 8.20 0.46 5.68 M L 8.15 0.37 4.51 –0.24 0.529 0.715 0.617 R 8.13 0.47 5.84

For explanations see Table 2. Objaśnienia jak w tabeli 2.

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Table 9. Statistical characteristics of the radius morphometrics in the raccoon dog Tabela 9. Charakterystyka statystyczna wymiarów kości promieniowej jenota

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed raccoon dog Jenot hodowlany F L 89.61 2.53 2.83 0.24 0.130 0.386 0.752 R 89.83 2.71 3.02 M L 91.63 1.71 1.87 0.39 0.091 0.386 0.752 R 91.99 1.79 1.94 Wild raccoon dog Jenot dziki F L 86.26 1.92 2.23 0.04 0.994 0.715 0.617 R 86.31 3.10 3.60 M L 84.75 5.41 6.38 2.47 –2.552 0.893 1.000 R 86.84 1.87 2.15 BP Farmed raccoon dog Jenot hodowlany F L 11.71 0.44 3.77 –2.30 –0.312 0.032* 0.343 R 11.45 0.38 3.30 M L 11.73 0.50 4.24 1.11 –0.333 0.285 0.343 R 11.86 0.42 3.56 Wild raccoon dog Jenot dziki F L 10.57 0.44 4.13 –0.18 –0.550 0.715 0.617 R 10.54 0.43 4.06 M L 10.70 0.40 3.79 0.64 –0.062 0.686 0.074 R 10.77 0.40 3.68 BD Farmed raccoon dog Jenot hodowlany F L 14.43 0.76 5.28 1.37 0.362 0.241 0.752 R 14.63 0.91 6.24 M L 15.11 0.74 4.93 0.60 –0.055 0.260 0.182 R 15.20 0.72 4.77 Wild raccoon dog Jenot dziki F L 13.96 0.68 4.85 1.28 –0.470 0.273 0.617 R 14.14 0.54 3.82 M L 14.56 0.44 3.02 1.33 –0.571 0.138 0.371 R 14.76 0.33 2.26 SD Farmed raccoon dog Jenot hodowlany F L 7.02 0.51 7.30 –0.95 –0.127 0.203 0.343 R 6.96 0.45 6.44 M L 7.18 0.37 5.23 –1.56 –0.454 0.154 0.114 R 7.07 0.30 4.23 Wild raccoon dog Jenot dziki F L 6.32 0.54 8.52 –0.31 0.034 0.144 0.612 R 6.13 0.55 8.94 M L 6.40 0.11 1.66 2.39 3.666 0.500 1.000 R 6.56 0.35 5.34 * – difference significant at P ≤ 0.05. * – różnica statystyczna na poziomie P ≤ 0,5.

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The asymmetry of selected$ 37 Table 10. Statistical characteristics of the ulna morphometrics in the raccoon dog

Tabela 10. Charakterystyka statystyczna wymiarów kości łokciowej jenota

Trait Cecha Origin Pochodzenie Sex Płeć Body side Strona ciała m (mm) SD V% RA FA TpW TZ GL Farmed raccoon dog Jenot hodowlany F L 108.68 3.56 3.28 0.20 –0.013 0.285 0.343 R 108.90 3.54 3.25 M L 111.51 2.32 2.08 0.30 –0.035 0.646 0.752 R 111.85 2.28 2.04 Wild raccoon dog Jenot dziki F L 102.11 6.53 6.40 0.21 0.080 0.465 0.617 R 102.32 6.83 6.67 M L 105.55 2.38 2.25 0.02 0.292 0.686 1.000 R 105.67 2.75 2.60 SDO Farmed raccoon dog Jenot hodowlany F L 12.57 0.43 3.45 4.88 1.033 0.007** 0.027* R 13.19 0.70 5.35 M L 12.99 0.54 4.18 1.89 0.218 0.139 0.114 R 13.24 0.60 4.57 Wild raccoon dog Jenot dziki F L 14.23 1.79 12.57 4.38 –5.535 0.465 0.617 R 14.86 0.32 2.16 M L 14.83 0.86 5.82 0.77 –1.044 0.500 1.000 R 14.95 0.52 3.50 DPA Farmed raccoon dog Jenot hodowlany F L 15.67 0.80 5.09 –0.10 –0.583 0.959 0.752 R 15.65 0.60 3.82 M L 15.62 0.69 4.39 1.02 –0.044 0.333 0.752 R 15.78 0.67 4.24 Wild raccoon dog Jenot dziki F L 13.04 0.54 4.13 –0.81 –0.750 0.715 0.617 R 12.93 0.38 2.93 M L 12.72 0.37 2.92 –1.43 –0.222 0.138 0.371 R 12.53 0.20 1.59 ** – difference significant at P ≤ 0.01. * – difference significant at P ≤ 0.05.

** – różnica statystyczna na poziomie P ≤ 0,01. * – różnica statystyczna na poziomie P ≤ 0,05.

Among the bones of the thoracic girdle in carnivores of a soft walk, the humerus is

particularly interesting due to the passive submission to the load of the body weight. Most

studies on the effect of symmetry and asymmetry of the bones constituting the pectoral girdle

and the bones of the forelimb concentrate on the analysis of their elements in bipedal

organisms, which use their upper limbs in manual activities. An example would be the

presence of left-sided asymmetry in the forelimb of captive chimpanzees (Hopkins 2008).

However, the factors predisposing to the formation of asymmetry include genetically determined

plasticity of the bones and some local agents, such as varying load, and differences in blood

supply and innervation. The data presented in Table 11 reveal directed asymmetries in

particular parts of the studied bones in both foxes and raccoon dogs. The presence of

incidental, statistically significant asymmetries can only be explained with variable, individual

manner of behavior, although there are reports on left-sided asymmetry in the hind limb of

dogs (Chase et al. 2004) and in red foxes, in which right-sided asymmetries in the humerus

and left-sided in the radius and the ulna have been found (Kharlamova et al. 2010).

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38 L. Felska-Błaszczyk et al.

Table 11. Number of left- and right-sided traits (total significant and non-significant) in females and males of the red foxes and raccoon dogs in the studied bones of the pectoral girdle

Tabela 11. Liczba cech lewo- i prawostronnych (istotnych i nieistotnych statystycznie razem) u samic i samców lisów i jenotów w badanych elementach szkieletu obręczy piersiowej

Origin Pochodzenie Scapula Łopatka Humerus Kość ramienna Radius Kość promieniowa Ulna Kość łokciowa F M F M F M F M L R L R L R L R L R L R L R L R FRF 1 4 1 4 3 4 7 0 1 3 2 2 0 3 2 1 WRF 4 1 4 1 6 1 7 0 3 1 2 2 2 1 0 3 FRG 1 4 3 2 6 1 2 5 2 2 1 3 1 2 0 3 WRD 3 2 2 3 3 4 2 5 2 2 0 4 1 2 1 2 Explanations: – Objaśnienia: L – left body side – lewa srona ciała; P – right body side – prawa strona ciała; FRF – farmed red fox – lis pospolity hodowlany; WRF – lis pospolity dziki; FRD – farmed raccoon dog – jenot hodowlany. WRD – wild raccoon dog – jenot dziki.

CONCLUSIONS

As a result of the study it can be concluded that the asymmetry of the forelimb bones

occurs sporadically and mainly in farmed animals. Origin and sex of the animals influenced

all the analyzed metric characteristics of selected bones. In the humerus of the red foxes we

found primarily left-sided asymmetry, which occurred frequently also in the dimensions of the

other analyzed bones. The statistical analysis of the impact of the side of the body on the

metric characters of the bones in raccoon dogs indicates the presence of asymmetry only

occasionally in the farmed animals. The results lead to a conclusion that the management of

furbearing animals under a shed housing system may lead to asymmetry in the skeleton

within the pectoral girdle.

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ACKNOWLEDGEMENTS

The study was financed by the National Centre for Research and Development (NCBiR),

grant no. 12-0140-10.

Abstract. The aim of the study was to determine the effect of origin and sex on the presence of symmetry or asymmetry in selected skeleton elements of the thoracic limb in wild and farmed fox and in wild and farmed raccoon dog. The study involved 20 farmed foxes (10 males and 10 females), 24 wild foxes (15 males and 9 females), 20 farmed raccoon dogs (10 males and

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40 L. Felska-Błaszczyk et al.

10 females) and 12 wild raccoon dogs (6 males and 6 females). The following right- and left-side skeletal parts of the pectoral girdle (cingulum membri thoracici) and the thoratic limb were dissected from all individuals: the shoulder blade (scapula), the humerus, the radius, and the ulna. The bones were measured using a digital caliper. The study showed that the asymmetry of the forelimb bones occurs sporadically and chiefly in farmed animals. The studied sources of variation (the origin of animals and sex) influenced all the analyzed metric characteristics of the bones. A left-sided asymmetry was found in the humeri of foxes, and was also present in the other skeletal parts. The results prompt a conclusion that the management of animals under the shed housing system may lead to asymmetry of the skeleton within the pectoral girdle.

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